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Sex in Penicillium: Combined Phylogenetic and Experimental Approaches

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Sex in Penicillium: Combined Phylogenetic and Experimental Approaches Fungal Genetics and Biology 47 (2010) 693–706 Contents lists available at ScienceDirect Fungal Genetics and Biology journal homepage: www.elsevier.com/locate/yfgbi Sex in Penicillium: Combined phylogenetic and experimental approaches M. López-Villavicencio a,*,1, G. Aguileta b,1, T. Giraud b, D.M. de Vienne a,b, S. Lacoste a, A. Couloux c, J. Dupont a a Origine, Structure, Evolution de la Diversité, UMR 7205 CNRS-MNHN, Muséum national d’histoire naturelle, CP39, 57 rue Cuvier, 75231 Paris Cedex 05, France b Ecologie, Systématique et Evolution, UMR 8079, Bâtiment 360, Université Paris-Sud, F-91405 Orsay cedex, France; UMR 8079, Bâtiment 360, CNRS, F-91405 Orsay cedex; France c Genoscope – Centre National de Séquençage: BP 191, 91006 EVRY cedex, France article info abstract Article history: We studied the mode of reproduction and its evolution in the fungal subgenus Penicillium Biverticillium Received 25 January 2010 using phylogenetic and experimental approaches. We sequenced mating type (MAT) genes and nuclear Accepted 6 May 2010 DNA fragments in sexual and putatively asexual species. Examination of the concordance between indi- Available online 9 May 2010 vidual trees supported the recognition of the morphological species. MAT genes were detected in two putatively asexual species and were found to evolve mostly under purifying selection, although high sub- Keywords: stitution rates were detected at some sites in some clades. The first steps of sexual reproduction could be Positive selection induced under controlled conditions in one of the two species, although no mature cleistothecia were Relaxed selection produced. Altogether, these findings suggest that the asexual Penicillium species may have lost sex only dN dS very recently and/or that the MAT genes are involved in other functions. An ancestral state reconstruction Talaromyces analysis indicated several events of putative sex loss in the genus. Alternatively, it is possible that the Experimental crosses supposedly asexual Penicillium species may have retained a cryptic sexual stage. Ó 2010 Published by Elsevier Inc. 1. Introduction appear to have had multiple transitions from sexuality to asexual- ity (Lobuglio et al., 1993). In Fungi, asexual reproduction by pro- Despite the costs of sex (Otto and Lenormand, 2002), most duction of asexual propagules (e.g. conidia) has been considered eukaryotes engage in sexual recombination at least at some point to be particularly common, with a quarter of fungal species in their life cycle. The predominance of sexual reproduction sug- thought to reproduce only by asexual means (Taylor et al., 1999). gests that sex must provide some advantages. Although asexual However, recent studies have shown that a great number of fungal reproduction is common in nature, exclusively asexual taxa are ‘‘asexual” species are in fact capable of sexual reproduction. Sex in rare and they are considered to be short-lived (Judson and these species is only difficult to observe in nature and challenging Normark, 1996). Many models have been built to explore short- to induce in the laboratory. Some species for which sex has not and long-term advantages of sex to explain its maintenance, but been observed, like Coccidioides immitis, present population struc- evidence from natural cases is still scarce (but see De Visser and tures consistent with recombination, suggesting the existence of Elena, 2007, for recent experimental evidence for direct benefits cryptic sex in nature (Burt et al., 1996). Sex has been successfully of sex). More information is needed on suitable biological models induced under controlled conditions in species such as Candida that could be used to tackle these issues. albicans (Hull et al., 2000), Aspergillus fumigatus (O’Gorman et al., The empirical study of sex and recombination has been based 2009), A. flavus and A. parasiticus, which were long thought to be on vertebrates, insects and plants models, while other groups of asexual (Horn et al., 2009a,b). Finally, apparently functional mating eukaryotes, including fungi, have been neglected (Birky, 1999). type genes (i.e. genes that define mating compatibility in fungi) Biological groups that exhibit a diversity of reproductive strategies have recently been identified and characterized in several species provide unique opportunities to study the evolution of sex. Groups with no sexual cycle described, such as A. oryzae (Galagan et al., such as fungi are thus excellent models as they present a great 2005), and recently in Penicillium chrysogenum and Acremonium range of reproductive strategies, including obligatory sexual spe- chrysogenum (Hoff et al., 2008; Pöggeler et al., 2008). Other fungal cies, those that alternate sexual and asexual reproduction, and oth- species shown to be truly clonal from a population genetic stand- ers that appear to be strictly asexual (Taylor et al., 1999). Fungi also point, such as Penicillium marneffei, also present mating type genes, suggesting that sex has been lost recently (Woo et al., 2006; Fisher, 2007). Alternatively, sexual reproduction that would always occur between identical clones, as allowed under homothallism, would * Corresponding author. Fax: +33 1 69 15 73 53. E-mail address: [email protected] (M. López-Villavicencio). not be distinguishable from strictly asexual reproduction using 1 Both authors contributed equally to this paper. population genetics. 1087-1845/$ - see front matter Ó 2010 Published by Elsevier Inc. doi:10.1016/j.fgb.2010.05.002 694 M. López-Villavicencio et al. / Fungal Genetics and Biology 47 (2010) 693–706 Besides the fact that Fungi represent suitable biological models mon descent. Most ascomycetes present two idiomorphs MAT 1- for studying the maintenance of sex and recombination, the study 1 and MAT 1-2. These genes code for transcription factors that in- of reproductive strategies in this group has important direct appli- duce the production of pheromones and pheromone receptors. The cations. Until very recently, many fungal plant pathogens and MAT 1-1 idiomorph includes a gene encoding a protein with a mo- some important animal pathogens and species with biotechnolog- tif called the a1 domain, while the MAT 1-2 idiomorph presents a ical importance were assumed to be clonal with widespread distri- gene encoding a protein with a DNA-binding domain similar to butions (Taylor et al., 1999). However, recent studies have revealed that of the high mobility group (HMG) (Coppin et al., 1997). Homo- the existence of recombination in some of these important species thallic fungi can undergo intra-haploid mating (Giraud et al., (Burt et al., 1996; Couch et al., 2005). Deciphering the mode of 2008), the proximal cause being in most of the filamentous homo- reproduction of pathogens may have profound implications for thallic ascomycetes, each haploid possesses two alternate forms of our understanding of the biology and for the management of the the MAT locus in its genome (Coppin et al., 1997). In contrast, het- species. Recombination should maintain genetic variation within erothallic fungi carry a single MAT idiomorph and two strains car- populations and generate new genotypes, which can present new rying complementary MAT idiomorphs are required for sex to or increased virulence, pathogenicity or drug resistance (Dyer occur. and Paoletti, 2005; Taylor et al., 1999). Furthermore, many of the Selective pressures acting on mating type genes are expected to fungi used in industry are thought to have only asexual reproduc- be different in sexual vs. asexual species, and these pressures can tion, and the discovery of a sexual stage could help improving be detected based on sequences (i.e. O’Donnell et al., 2004). In sex- strain quality by crosses (Pöggeler, 2001). ually reproducing species, mating type genes must remain func- Here, we studied the evolution of reproduction in the fungal tional in order for sex to take place, implying that purifying subgenus Penicillium Biverticillium using phylogenetic and experi- selection should act (Devier et al., 2009; O’Donnell et al., 2004). mental approaches. This group includes important species, such On the other hand, in asexual species still carrying mating type as the opportunistic pathogen P. marneffei, food and feed spoilers genes, mutations driving loss of function should be selectively neu- as well as species of importance in the food and biotechnology tral (Fisher, 2007), leading to relaxed selection. Positive selection industries, such as P. pinophilum and P. funiculosum (Domsch et al., may act on MAT genes in sexual species, involving rapid and recur- 1980). In the fungal genus Penicillium counting ca. 250 species (Pitt, rent changes that proved advantageous (Wik et al., 2008). We 1979), only few species have a complete life cycle described, the therefore looked for footprints of acceleration in substitution rates teleomorphs being then Talaromyces or Eupenicillium. The remain- (indicating relaxed selection or positive selection) on MAT genes. ing species are considered as strictly asexual fungi, corresponding Finally, when species were found to have both MAT 1-1 and MAT to several independent losses of sex (Lobuglio et al., 1993). Asexual 1-2 alleles, we attempted to induce a sexual cycle experimentally. species have been classified into four subgenera, Aspergilloides, Biverticillium, Penicillium and Furcatum on the base of the morphol- 2. Material and methods ogy of their penicilli (Pitt, 1979). The subgenus Biverticillium is phylogenetically related to Talaromyces (Lobuglio et al.,
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